Interspecific differences in snail susceptibility to crab predation at
Jakobsen’s Beach, Lake Tanganyika
Student: Anne M. Socci
Mentor: Dr. Ellinor Michel
Introduction
The robust crushing chelae of durophagous crabs in Lake Tanganyika and the heavily calcified and ornate
shells of endemic thiarid gastropods have been identified as highly derived coevolutionary adaptations to
predator-prey interactions between the two taxa (West and Cohen 1994, West et al. 1991). There is a
striking diversity of adaptations among gastropods in the lake that signal the evolution of unique intra- and
inter-generic morphologies and behaviors as strategies for predator defense (West and Cohen, 1996).
Past research on gastropod vulnerability to crab predation provides evidence that increased shell height
(length) and apertural lip thickening decreased the vulnerability of certain gastropod species and
individuals within a species to shell crushing (West et al. 1991). Research up to this point, however, has
not eliminated variation in snail size when making interspecific comparisons of prey susceptibility. In
addition, there is little known about interspecific differences in durophagous crab predators. The purpose
of this study was to examine interspecific differences in susceptibility in snails and interspecific differences
in predation success in crabs using a series of predation trials in the laboratory and by surveying scar
frequency in a one area in Lake Tanganyika.
Methods
Study Site
We collected all snails and crabs along a 300 m stretch of the rocky littoral zone of Jakobsen’s Bay’s south
rim (4° 54.64’ S, 29° 35.92’ E), located 5 km south of Kigoma, Tanzania. Jakobsen’s Bay is surrounded by
undeveloped shoreline and can be considered relatively pristine. We obtained individuals at 1-12m depth
using a combination of snorkel and SCUBA.
Gastropod Measurement Protocol (adapted from Cohen 1989)
A single person took all measurements of gastropods and crabs with the same set of Fowler Ultracal III
digital calipers linked directly to a computer spreadsheet. We took the following set of measurements for
all individuals used in this study:
Conic gastropods Lavigeria coronata, L. grandis, L. new sp. M, L. nassa, Nov. gen. guillemei, Reymondia
horei.
1) Height. Maximum height measured from the apex to the basal inflection of the aperture.
2) Width. Maximum width of shell and any extensions of shell sculpture measured perpendicular
to Height.
3) Lip thickness. Apertural lip thickness measured at the widest point of the lower and outer
apertural inflection, with calipers inserted a standard 2mm from the lip and between horizontal
ribs.
4) Aperture-apex. Preapertural height measured from the upper intersection of the last whorl at
the aperture to the apex.
5) Scar-apex. Preapertural height of the individual at the time of scarring. Measured at the upper
intersection of the scarred whorl at what would have been the aperture at the time of scarring.
Button-shaped gastropod Spekia zonata.
1) Height. Maximum height along an imaginary axis of coiling from the top of the apex to the
lowest point of the outer edge of the aperture.
2) Width. Maximum width perpendicular to Height.
3) Lip thickness. Apertural lip thickness measured at the widest point of the lower and outer
apertural inflection, with calipers inserted a standard 2mm from the lip.
Crabs Platytelphusa armata and Potamonautes platynotus).
1) Carapace width. Maximum width of the carapace excluding spines or extensions in shell
sculpture.
2) Left and right chelae diagonal. Maximum diagonal distance between the tip of the lower joint
of the claw and the small spherical articulation at the joint between the upper cheliped and the
limb (excluding the spines on the articulation in P. armata).
Crab Predation Trials
In order to observe the physical ability of crabs to prey upon snails in the absence of physical refugia for
the snails or alternative and potentially more preferable food resources for the crab, we conducted crab
predation trials in the laboratory using six species of snails that are relatively abundant at Jakobsen’s beach:
Lavigeria coronata, L. grandis, L. nassa, L. new sp. M, Spekia zonata, and Reymondia horei, and two
species of snail-eating crabs also abundant at Jakobsen’s: Platytelphusa armata and Potamonautes
platynotus. In order to control for size differences between snail species as a predation variable, we
collected individuals that were comparable in size across the six species, typically juveniles of L. coronata,
L. nassa, L. grandis, and S. zonata, and adults of R. horei, and L. new sp. M. We collected crabs daily
using wire mesh traps set at depths ranging from 1-8 meters and baited with raw meat, and held the crabs in
aquaria in the laboratory for a 24-72 hour acclimation period.
We measured the height, width, lip thickness, and aperture-apex distance of each snail used in the
experiment, and the carapace width, and left and right chelae diagonal distance of each crab. We also
recorded the presence or absence of adult modification in the snails in the form of a thickened aperture lip,
as this would presumably influence the crab’s ability to crush or peel the shell. In addition, we recorded the
sex of each crab and the “molarity” of each crab’s major chela. Using a scale of one to three, “molarity”
was a relative measure of the extent to which the major chela had a differentiated molariform morphology.
Major chelae with undifferentiated pointed spikes or worn down differentiated “teeth” were scored with a
one. Major chelae with a combination of differentiated “teeth” and spikes, or only partially worn “teeth”
were scored with a two. Major chelae with fully differentiated “teeth” analogous to human molars and
premolars were scored with a three. We excluded gravid female crabs from the trials.
We conducted ten trial blocks between 18 and 29 July 2001. Each trial consisted of six individuals each of
P. armata and P. platynotus randomly assigned to one individual of L. coronata, L. grandis, L. nassa L.
new sp. M, S. zonata, and R. horei. During the trial we held each crab in clear plastic 2 L chambers
holding 1.5 L of water aerated constantly throughout the trial. Trials lasted 18 hours- 13 hours in darkness
and 6 hours in light. At the end of the trial period, we removed crabs from the chambers and recorded the
status of the snail as dead, damaged, or unharmed. Snail death in every case meant a successful predation
by the crab, in which the shell was crushed and the soft tissue eaten. Snail damage meant an unsuccessful
predation attempt, in which the succeeded in peeling back a portion of the lip of the snail shell, but did not
kill and eat the snail. A snail was considered to be unharmed if it was found alive in the chamber with no
evidence of shell damage.
We used all individual crabs and snails for only one trial, and afterwards either returned individuals to
Jakobsen’s Bay or preserved them for separate analyses. In order to avoid accidental re-use of crab
individuals, we marked each crab with a numbered bee tag, super-glued on the carapace prior to release.
Scar Frequency Survey
We conducted our scar frequency survey on seven species of snails collected from the rocky littoral zone of
the southern rim of Jakobsen’s Bay: Lavigeria coronata, L. grandis, L. nassa, L. new sp M, Spekia zonata,
Reymondia horei, and Nov.gen. guillemei. We collected 300 individuals of each species between 22 July8 August, and scrubbed algae from the shells in order to improve visibility of scars and shell characteristics
prior to measuring the height, width, lip thickness and aperture-apex distance of each individual. In
addition to these measurements, we noted the presence or absence of adult modification in the form of lip
thickening in each individual. For scarred individuals we measured the scar-apex distance of each scar.
Following measurement we returned individuals to Jakobsen’s Bay or recycled them for separate analyses.
Data were tested for differences in scarring frequency and size at scarring between snail species. All
analyses were performed using SYSTAT (Version 7.0, SPSS Inc., 1997).
Soft Body Mass to Shell Mass Ratio Analysis
We conducted the soft body mass to shell mass ratio analysis on seven species of snails collected at
Jakobsen’s Bay: Lavigeria coronata, L. grandis, L. nassa, L. new sp. M, Spekia zonata, Reymondia horei,
and Nov. gen. guillemei. We selected a juvenile-adult stage size series of 30 unscarred individuals of each
species from individuals collected between 18 July-5 August 2001 using a combination of snorkel and
SCUBA at 1-12m depth. We held individuals in aquaria for a minimum of 24 hours after collection so that
gut contents would be excreted prior to analysis. Following this period we blotted excess water from the
shells and preserved individuals by freezing them.
Prior to separating the soft body from the shell, we measured the height, width, lip thickness, and apertureapex distance of every individual. In addition, we recorded the presence or absence of adult modification
in the form of lip thickening. Following measurement we cracked the shell of each individual using a table
vice, separated soft tissue from the shell, and removed the operculum and discarded it. In the case of
gravid females, we separated brooded young with calcareous shells and measured them individually. We
then dried the soft tissue and the shell fragments of each individual separately from one another in a drying
oven at 60 degrees Celsius. Once dry, we recorded the mass of the soft tissue and shell of each individual.
Results
Crab Predation Trials
Across trials with all six species of snails, Platytelphusa armata caused significantly higher mortality than
Platypotamonautes platynotus (Mantel Haenszel statistic = 2.319, Mantel Haenszel chi square = 4.305, p=
0.038). This analysis controls for differences between snail species in overall susceptibility. Speciesspecific tests of differences in crab predation were significant only for Lavigeria nassa and L. coronata, in
which P. armata caused higher mortality than P. platynotus (L. nassa: Pearson chi square = 5.051, df=1,
p=0.025; L. coronata: Pearson chi square=7.5, df=1, p=0.006; Figure 1).
Individual tests of differences in snail susceptibility between two snail species show that Reymondia horei
had significantly lower mortality when compared to L. nassa, L. grandis, and L. new sp. M (L. nassa:
Pearson chi square =6.667, df=1, p=.01; L. grandis: Pearson chi square =8.286, df=1, p=.004; L. new sp.
M: Pearson chi square= 3.956, df=1, p=.004).
Scar Frequency Survey
Lavigeria nassa, L. coronata, and L. grandis had no significant differences in scarring frequency between
one another, but did have significant differences in scarring frequency when compared to the other four
species. These three species of Lavigeria had high scarring frequencies, while L. new sp. M had an
extremely low scarring frequency (Figure 2).
Soft Body Mass to Shell Mass Ratio Analysis
The body mass to shell mass data showed surprisingly similar relationships among species. Spekia
exhibited elevated body mass to shell height (Figure 3). Results from L. new sp. M were not interpretable
and are not plotted. Nov. gen. guillemei dry weight was unusually high.
Figure 1
1
0.9
0.8
Mortality
0.7
Platytelphusa armata
*
Potamonautes platynotus
Platypotamonautes
platynotus
*
*
0.6
0.5
0.4
0.3
0.2
0.1
0
L. nassa
L. coronata
L. grandis
L. new sp. M
R. horei
S. zonata
Snail Species
Figure 2
Scar Frequency
0.60
0.50
0.40
0.30
0.20
0.10
0.00
L.nassa
L.coronata
L.grandis
L.new sp. M
Snail Species
Nov.gen.
guillemei
R. horei
S. zonata
Figure 3
1
1
0
Y
R
-1
D
G
O -2
L
SPECIES
spekia
reymondia
nassa
grandis
coronata
NovGen
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LOGSHELL
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spekia
reymondia
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0.8 1.0 1.2
LOGHEIGHT
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NovGen
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LOGDRY
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LOGSHELL
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spekia
reymondia
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NovGen
L.sp.M
1.4
1.6
spekia
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NovGen
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Discussion
The low mortality in the crab predation trials of a species such as Reymondia horei, which is relatively
small in size with a smooth shell lacking in significant shell calcification, is quite striking when compared
to the relatively high mortality of species with highly sculptured shells such as Lavigeria coronata and
Lavigeria nassa. Snails used in these trials were relatively small, and none of the individuals of the large,
well-armored Lavigeria species were large enough to exhibit adult modification in the form of apertural lip
thickening. At that size, therefore, it appears that Reymondia’s shell morphology provides better defense
from predation than that of the other species used in this experiment.
In the scar frequency data there is a strong contrast between the large, heavily calcified Lavigeria species
and the smaller, thin-shelled L. new sp. M. The low scarring frequency of L. new sp. M. can be interpreted
in two ways. Either it is less common as a desired prey item, or it less frequently survives an attack.
The body mass to shell mass data showed surprisingly consistent relationships both among and within
species. The distinctive regressions for Spekia are likely to be due to how height meausures correlate with
overall shell size. The geometry of these button-shaped shells is so different from the conic shells that this
is not a comparable measure. A multivariate size measure combining height and width might make this
more comparable. The unusually high dry weight relationship of Nov. gen. guillemei is not easily
explained, as these animals look similar to other conic gastropods, do not contain broods (and the elevated
dry weight holds for both males and females). Otherwise, there is no obvious pattern of species differences
in soft tissue relative to shell mass that could help interpret the differences in either experimental or scar
frequency predation data.
In all cases of species used in this experiment, future research on behavioral strategies in the field are
imperative to understanding the interplay between structural shell morphology and predator avoidance
behavior in understanding the effectiveness of each species’ evolutionary strategies for surviving crab
predation pressure.
Acknowledgements
I would like to thank my mentor, E. Michel, for her invaluable insight, support, and endless supply of
Mama Moez’s goodies. I likewise thank P. McIntyre for his dedication to our projects, statistical prowess,
and all-around good nature. Thanks to the rest of Team Bio- C. Solomon, A. Rivers, and K. Hinkley for
their hard work and support. And, finally, thanks to every member of Nyanza 2001 for keeping me fed!
This work would not have been possible without the generous support of the National Science Foundation,
NSF grant ATM 9619458.
References
Cohen, A.S., 1989. The taphonomy of gastropod shell accumulations in large lakes: an example from Lake
Tanganyika, Africa. Paleobiology 15: 26-45.
Cumberlidge, N. R. von Sternberg, R. Bills, and H. Martin, 1999. A revision of the genus Platytelphusa A.
Milne-Edwards 1887 from Lake Tanganyika, East Africa (Decapoda: Potamoidea: Platytelphusidae).
Journal of Natural History 33: 1487-1512.
West, K., A. Cohen, and M. Baron, 1991. Morphology and behavior of crabs and gastropods from Lake
Tanganyika, Africa: Implications for lacustrine predator-prey coevolution. Evolution 45:589-607.
West,K. and A. Cohen, 1994. Predator-prey coevolution as a model for the unusual Morphologies of the
crabs and gastropods of Lake Tanganyika. Ergebnisse der Limnologie 0(44): 267-283.
West, K. and Cohen, A., 1996. Shell microstructure of gastropods from Lake Tanganyika, Africa:
Adaptation, convergent evolution and escalation. Evolution 50(2):672-681.
Figure Captions
Figure 1. Snail mortality by Platytelphusa armata and Potamonautes platynotus during ten predation
trials. A * symbol denotes a significant difference between mortality caused by P. armata and
mortality caused by P. platynotus for a particular snail species (p<.05).
Figure 2. Scar frequency of seven species of thiarid gastropods collected at 1-12m depth in Jakobsen's Bay,
Lake Tanganyika (Sample size: L.nassa, n=327; L. coronata, n= 160; L. grandis, n=326; L.new
sp. M, n=300; Nov. gen. guillemei, n=335; Reymondia horei, n=301; Spekia zonata, n=305).
Figure 3. Body mass to shell mass relationships. a) Log shell weight vs. log dry body weight, b) Log shell
height vs. log dry body weight, c) Log shell height vs. log wet body weight, d) Log shell height vs.
log shell weight, e) log wet body weight vs. log dry body weight.